Populations Of Threespine Stickleback Research Articles

Evolution of Schooling Behavior in Threespine Sticklebacks Is Shaped by the Eda Gene.

Despite longstanding interest in the genetic mechanisms that underlie behavioral evolution, very few genes that underlie naturally occurring variation in behavior between individuals or species are known, particularly in vertebrates. Here, we build on our previous forward genetic mapping experiments and use transgenic approaches to identify Ectodysplasin as a gene that causes differences in schooling behavior between wild populations of threespine stickleback (Gasterosteus aculeatus) fish. This work provides rare insight into the proximate mechanisms that have shaped the evolution of vertebrate behavior.

Conserved effects of salinity acclimation on thermal tolerance and hsp70 expression in divergent populations of threespine stickleback (Gasterosteus aculeatus)

In natural environments, organisms must cope with complex combinations of abiotic stressors. Here, we use threespine stickleback (Gasterosteus aculeatus) to examine how changes in salinity affect tolerance of high temperatures. Threespine stickleback inhabit a range of environments that vary in both salinity and thermal stability making this species an excellent system for investigating interacting stressors. We examined the effects of environmental salinity on maximum thermal tolerance (CTMax) and 70kDa heat shock protein (hsp70) gene expression using divergent stickleback ecotypes from marine and freshwater habitats. In both ecotypes, the CTMax of fish acclimated to 20 ppt was significantly higher compared to fish acclimated to 2 ppt. The effect of salinity acclimation on the expression of hsp70-1 and hsp70-2 was similar in both the marine and freshwater stickleback ecotype. There were differences in the expression profiles of hsp70-1 and hsp70-2 during heat shock, with hsp70-2 being induced earlier and to a higher level compared to hsp70-1. These data suggest that the two hsp70 isoforms may have functionally different roles in the heat shock response. Lastly, acute salinity challenge coupled with heat shock revealed that the osmoregulatory demands experienced during the heat shock response have a larger effect on the hsp70 expression profile than does the acclimation salinity.

Rapid adaptive evolution of colour vision in the threespine stickleback radiation.

Vision is a sensory modality of fundamental importance for many animals, aiding in foraging, detection of predators and mate choice. Adaptation to local ambient light conditions is thought to be commonplace, and a match between spectral sensitivity and light spectrum is predicted. We use opsin gene expression to test for local adaptation and matching of spectral sensitivity in multiple independent lake populations of threespine stickleback populations derived since the last ice age from an ancestral marine form. We show that sensitivity across the visual spectrum is shifted repeatedly towards longer wavelengths in freshwater compared with the ancestral marine form. Laboratory rearing suggests that this shift is largely genetically based. Using a new metric, we found that the magnitude of shift in spectral sensitivity in each population corresponds strongly to the transition in the availability of different wavelengths of light between the marine and lake environments. We also found evidence of local adaptation by sympatric benthic and limnetic ecotypes to different light environments within lakes. Our findings indicate rapid parallel evolution of the visual system to altered light conditions. The changes have not, however, yielded a close matching of spectrum-wide sensitivity to wavelength availability, for reasons we discuss.

Investment in boney defensive traits alters organismal stoichiometry and excretion in fish.

Understanding how trait diversification alters ecosystem processes is an important goal for ecological and evolutionary studies. Ecological stoichiometry provides a framework for predicting how traits affect ecosystem function. The growth rate hypothesis of ecological stoichiometry links growth and phosphorus (P) body composition in taxa where nucleic acids are a significant pool of body P. In vertebrates, however, most of the P is bound within bone, and organisms with boney structures can vary in terms of the relative contributions of bones to body composition. Threespine stickleback populations have substantial variation in boney armour plating. Shaped by natural selection, this variation provides a model system to study the links between evolution of bone content, elemental body composition, and P excretion. We measure carbon:nitrogen:P body composition from stickleback populations that vary in armour phenotype. We develop a mechanistic mass-balance model to explore factors affecting P excretion, and measure P excretion from two populations with contrasting armour phenotypes. Completely armoured morphs have higher body %P but excrete more P per unit body mass than other morphs. The model suggests that such differences are driven by phenotypic differences in P intake as well as body %P composition. Our results show that while investment in boney traits alters the elemental composition of vertebrate bodies, excretion rates depend on how acquisition and assimilation traits covary with boney trait investment. These results also provide a stoichiometric hypothesis to explain the repeated loss of boney armour in threespine sticklebacks upon colonizing freshwater ecosystems.

Cryptic invasion drives phenotypic changes in central European threespine stickleback

Cryptic invasions are commonly associated with genetic changes of the native species or genetic lineage that the invaders replace. Phenotypic shifts resulting from cryptic invasions are less commonly reported given the relative paucity of historical specimens that document such phenotypic changes. Here, I study such a case in two populations of threespine stickleback from central Europe, comparing contemporary patterns of gene flow with phenotypic changes between historical and contemporary population samples. I find gene flow from an invasive lineage to be associated with significant phenotypic changes, where the degree of phenotypic change corresponds with the level of gene flow that a population receives. These findings underline the utility of combining genetic approaches with phenotypic data to estimate the impact of gene flow in systems where anthropogenic alterations have removed former geographic barriers promoting cryptic invasions.

Environmental change disrupts communication and sexual selection in a stickleback population.

Environmental change that disrupts communication during mate choice and alters sexual selection could influence population dynamics. Yet little is known about such long-term effects. We investigated experimentally the consequences that disrupted visual communication during mate choice has for the quantity and viability of offspring produced in a threespine stickleback population (Gasterosteus aculeatus). We further related the results to long-term monitoring of population dynamics in the field to determine if changes are apparent under natural conditions. The results show that impaired visual communication because of algal blooms reduces reliability of male visual signals as indicators of offspring survival during their first weeks of life. This relaxes sexual selection but has no effect on the number of offspring hatching, as most males have a high hatching success in turbid water. Despite eutrophication and high turbidity levels that interfere with communication during mate choice, the population has grown during recent decades. Large numbers of offspring hatching, combined with high variation in juvenile fitness, has probably shifted selection to later life history stages and maintained a viable population. Together with reduced cost of sexual selection and ongoing ecosystem changes caused by human activities, this could have promoted population growth. These results point to the complexity of ecosystems and the necessity to consider all influencing factors when attempting to understand impacts of human activities on populations.

An Empirical Test of Metabolic Effects and Adaptive Potential in Response to Global Ocean Warming in a Model Fish Species, the Threespine Stickleback

Climate change has had a significant influence on the world's oceans, which have shown constant increases in mean water temperature over the last 50 years. The biota of Arctic environments, ectotherms in particular, may be particularly threatened by this change: whilst southern animals have the possibility of migrating north, those adapted to colder northern climes have nowhere left to move and may be faced with the ‘choice’ of adapt or die. A key factor in adaptation to the changing thermal environment is the physiological response. Metabolic scope (the difference between minimum and maximum oxygen consumption rate) is likely a key fitness related trait because it defines energy available for locomotion, growth and reproduction. The unifying aim of our research is to develop a deeper understanding of the constraints and/or adaptive potential in metabolic scope with respect to thermal changes predicted due to climate change.As obligate ectotherms, threespine stickleback (Gasterosteus aculeatus) populations adapted to localized thermal conditions provide an excellent and logistically tractable model for study of thermal and metabolic evolution in a changing environment. We collected broodstock from anadromous Barents Sea fish and bred them under controlled conditions for two generations to standardize environmental & maternal sources of variance. The multi‐generational pedigree and large numbers of families (N=180, 40 families) permits estimation of additive genetic variance, whereas repeated measurements in multiple environments allows us to estimate direct environmental variance on metabolism and swimming performance. Maximum and minimum metabolic rates, in addition to critical swimming performance, were measured with the same individuals at three different temperatures: (i) contemporary summer temperature for Barents Sea coastal waters (12°C), (ii) extreme predictions under global warming (17°C), and (iii) stressful temperature (80% of CTmax). Individual critical temperature in observed population varied between 27.2 and 32.1°C. The preliminary results showed that minimum and maximum metabolic rates increased with the temperature rise: 61.6 ± 10.1 and 126.2 ± 36.1 mg O2/kg/hour at 12°C; 70.19 ± 11.8 and 144.9 ± 38.8 mg O2/kg/hour at 17°C; 114.0 ± 15.7 and 183.7 ± 32.0 mg O2/kg/hour at individual stressful temperature, respectively. However, the highest aerobic metabolic scope and swimming performance were observed at 17°C. Quantitative genetic analyses are ongoing, but point to the broad potential for adaptation to environmental change.Support or Funding InformationSM: Alfred Cordelin Foundation, Otto A. Malm Foundation, Oscar Öflund Foundation, LUOVA doctoral programme; RJSM, JM, TM: Academy of Finland

Stoichiometry of Novel Protein Modifications in Livers of Warm‐adapted Threespine Sticklebacks from Baja California (Mexico)

The purpose of this study was to investigate molecular phenotypes that have enabled the survival of a species above its typical lethal temperature limit. A unique population of threespine sticklebacks (Gasterosteus aculeatus) from Baja California, Mexico are surviving and able to function normally at temperatures close to 30 degrees Celsius, a temperature that is higher than normal for this species. Understanding how this warm‐adapted population is able to function at high temperatures at the molecular level may give insight into the mechanisms that have allowed for their survival, and the potential for other populations to adapt to increasing temperatures due to global climate change. Livers from sticklebacks of this unique warm‐adapted population (Baja California, Mexico) were compared to those of a typical cold‐adapted population (Anchorage, Alaska) using gel‐free quantitative proteomics by liquid chromatography‐mass spectrometry (LC‐MS/MS) in order to identify post‐translational modifications (PTMs) in proteins involved in redox and detoxifying biochemical pathways. The stoichiometry of these proteins were then compared between the two populations. Nineteen novel PTMs were identified in 11 different redox proteins, with major differences in stoichiometry detected between the two populations for catalase, alcohol dehydrogenase 1, three glutathione‐s‐transferase isozymes, and carbonyl reductase [NADPH] 1. Further investigation into the functional significance of these PTMs has the potential to reveal novel mechanisms by which adaptation to high temperatures affects redox regulation and detoxification mechanisms. It is well known that adaptation to high temperature affects gene and protein sequences at evolutionary time‐scales and the expression of abundances of particular mRNAs and proteins. Our study provides evidence that specific covalent protein modifications also represent important targets of evolutionary selection during high temperature adaptation of fish. Such modifications result in modulation of protein structure and function leading to concomitant changes in molecular and higher‐order phenotypes that provide an apparent adaptive advantage at elevated habitat temperature.Support or Funding InformationThis work was supported by the National Science Foundation, IOB 1355098.

Whole-genome sequencing reveals small genomic regions of introgression in an introduced crater lake population of threespine stickleback.

Invasive species pose a major threat to biological diversity. Although introduced populations often experience population bottlenecks, some invasive species are thought to be originated from hybridization between multiple populations or species, which can contribute to the maintenance of high genetic diversity. Recent advances in genome sequencing enable us to trace the evolutionary history of invasive species even at whole‐genome level and may help to identify the history of past hybridization that may be overlooked by traditional marker‐based analysis. Here, we conducted whole‐genome sequencing of eight threespine stickleback (Gasterosteus aculeatus) individuals, four from a recently introduced crater lake population and four of the putative source population. We found that both populations have several small genomic regions with high genetic diversity, which resulted from introgression from a closely related species (Gasterosteus nipponicus). The sizes of the regions were too small to be detected with traditional marker‐based analysis or even some reduced‐representation sequencing methods. Further amplicon sequencing revealed linkage disequilibrium around an introgression site, which suggests the possibility of selective sweep at the introgression site. Thus, interspecies introgression might predate introduction and increase genetic variation in the source population. Whole‐genome sequencing of even a small number of individuals can therefore provide higher resolution inference of history of introduced populations.

Habitat choice and female preference in a polymorphic stickleback population

Background: A small pond, c. 90 years old, near Bern, Switzerland contains a population of threespine stickleback (Gasterosteus aculeatus) with two distinct male phenotypes. Males of one type are large, and red, and nest in the shallow littoral zone. The males of the other are small and orange, and nest offshore at slightly greater depth. The females in this population are phenotypically highly variable but cannot easily be assigned to either male type. Question: Is the existence of two sympatric male morphs maintained by substrate-associated male nest site choice and facilitated by female mate preferences? Organisms: Male stickleback caught individually at their breeding sites. Females caught with minnow traps. Methods: In experimental tanks, we simulated the slope and substrate of the two nesting habitats. We then placed individual males in a tank and observed in which habitat the male would build his nest. In a simultaneous two-stimulus choice design, we gave females the choice between a large, red male and a small, orange one. We measured female morphology and used linear mixed effect models to determine whether female preference correlated with female morphology. Results: Both red and orange males preferred nesting in the habitat that simulated the slightly deeper offshore condition. This is the habitat occupied by the small, orange males in the pond itself. The proportion of females that chose a small orange male was similar to that which chose a large red male. Several aspects of female phenotype correlated with the male type that a female preferred.

Genetic basis for body size variation between an anadromous and two derived lacustrine populations of threespine stickleback Gasterosteus aculeatus in southwest Alaska.

Body size is a highly variable trait among geographically separated populations. Size-assortative reproductive isolation has been linked to recent adaptive radiations of threespine stickleback (Gasterosteus aculeatus) into freshwater, but the genetic basis of the commonly found size difference between anadromous and derived lacustrine sticklebacks has not been tested. We studied the genetic basis of size differences between recently diverging stickleback lineages in southwest Alaska using a common environment experiment. We crossed stickleback within one anadromous (Naknek River) and one lake (Pringle Lake) population and between the anadromous and two lake populations (Pringle and JoJo Lakes), and raised them in a salinity of 4–6 ppt. The F1 anadromous and freshwater forms differed significantly in size, whereas hybrids were intermediate or exhibited dominance toward the anadromous form. Additionally, the size of freshwater F1s differed from their wild counterparts, with within-population F1s from Pringle Lake growing larger than their wild counterparts, while there was no size difference between lab-raised and wild anadromous fish. Sexual dimorphism was always present in anadromous fish, but not in freshwater, and not always in the hybrid crosses. These results, along with parallel changes among anadromous and freshwater forms in other regions, suggest that this heritable trait is both plastic and may be under divergent and/or sexual selection.

Natural variation in brain gene expression profiles of aggressive and nonaggressive individual sticklebacks.

Within many species, some individuals are consistently more aggressive than others. We examine whether there are differences in brain gene expression between aggressive versus nonaggressive behavioural types of individuals within a natural population of male three-spined sticklebacks (Gasterosteus aculeatus). We compared gene expression profiles of aggressive male sticklebacks to nonaggressive males in four regions of the brain (brainstem, cerebellum, diencephalon and telencephalon). Relatively few genes were differentially expressed between behavioural types in telencephalon, cerebellum and diencephalon, but hundreds of genes were differentially expressed in brainstem, a brain area involved in detecting threats. Six genes that were differentially expressed in response to a territorial intrusion in a previous study were also differentially expressed between behavioural types in this study, implying primarily non-shared but some shared molecular mechanisms. Our findings offer new insights into the molecular causes and correlates of behavioural plasticity and individual variation in behaviour.

Innate immune responses to gut microbiota differ between oceanic and freshwater threespine stickleback populations.

ABSTRACTAnimal hosts must co-exist with beneficial microbes while simultaneously being able to mount rapid, non-specific, innate immune responses to pathogenic microbes. How this balance is achieved is not fully understood, and disruption of this relationship can lead to disease. Excessive inflammatory responses to resident microbes are characteristic of certain gastrointestinal pathologies such as inflammatory bowel disease (IBD). The immune dysregulation of IBD has complex genetic underpinnings that cannot be fully recapitulated with single-gene-knockout models. A deeper understanding of the genetic regulation of innate immune responses to resident microbes requires the ability to measure immune responses in the presence and absence of the microbiota using vertebrate models with complex genetic variation. Here, we describe a new gnotobiotic vertebrate model to explore the natural genetic variation that contributes to differences in innate immune responses to microbiota. Threespine stickleback, Gasterosteus aculeatus, has been used to study the developmental genetics of complex traits during the repeated evolution from ancestral oceanic to derived freshwater forms. We established methods to rear germ-free stickleback larvae and gnotobiotic animals monoassociated with single bacterial isolates. We characterized the innate immune response of these fish to resident gut microbes by quantifying the neutrophil cells in conventionally reared monoassociated or germ-free stickleback from both oceanic and freshwater populations grown in a common intermediate salinity environment. We found that oceanic and freshwater fish in the wild and in the laboratory share many intestinal microbial community members. However, oceanic fish mount a strong immune response to residential microbiota, whereas freshwater fish frequently do not. A strong innate immune response was uniformly observed across oceanic families, but this response varied among families of freshwater fish. The gnotobiotic stickleback model that we have developed therefore provides a platform for future studies mapping the natural genetic basis of the variation in immune response to microbes.

Different behaviour-body length correlations in two populations of juvenile three-spined stickleback (Gasterosteus aculeatus)

Behavioural variation among individuals has received a lot of attention by behavioural ecologists in the past few years. Its causes and consequences are becoming vast areas of research. The origin and maintenance of individual variation in behaviour within and among populations is affected by many facets of the biotic and abiotic environment.Here, two populations of lab-reared juvenile three-spined sticklebacks (Gasterosteus aculeatus) are tested for three behaviours (boldness, exploration, and sociability). Given the identical rearing conditions, the only difference between these populations is the parental habitat. In both populations, correlations between behaviour and body length are found. Interestingly, these differ between the populations. In one population body length was negatively correlated with exploratory behaviour, while in the other one body length correlated negatively with sociability.Considering the identical environment these juvenile fish were exposed to, these findings suggest a potential (epi)genetic foundation for these correlations and shows that, in three-spined sticklebacks, the proximate basis for correlations between body length and behaviour appears quite malleable.

The impact of selection, gene flow and demographic history on heterogeneous genomic divergence: three-spine sticklebacks in divergent environments.

Heterogeneous genomic divergence between populations may reflect selection, but should also be seen in conjunction with gene flow and drift, particularly population bottlenecks. Marine and freshwater three-spine stickleback (Gasterosteus aculeatus) populations often exhibit different lateral armour plate morphs. Moreover, strikingly parallel genomic footprints across different marine-freshwater population pairs are interpreted as parallel evolution and gene reuse. Nevertheless, in some geographic regions like the North Sea and Baltic Sea, different patterns are observed. Freshwater populations in coastal regions are often dominated by marine morphs, suggesting that gene flow overwhelms selection, and genomic parallelism may also be less pronounced. We used RAD sequencing for analysing 28 888 SNPs in two marine and seven freshwater populations in Denmark, Europe. Freshwater populations represented a variety of environments: river populations accessible to gene flow from marine sticklebacks and large and small isolated lakes with and without fish predators. Sticklebacks in an accessible river environment showed minimal morphological and genomewide divergence from marine populations, supporting the hypothesis of gene flow overriding selection. Allele frequency spectra suggested bottlenecks in all freshwater populations, and particularly two small lake populations. However, genomic footprints ascribed to selection could nevertheless be identified. No genomic regions were consistent freshwater-marine outliers, and parallelism was much lower than in other comparable studies. Two genomic regions previously described to be under divergent selection in freshwater and marine populations were outliers between different freshwater populations. We ascribe these patterns to stronger environmental heterogeneity among freshwater populations in our study as compared to most other studies, although the demographic history involving bottlenecks should also be considered in the interpretation of results.

Development of a Bioenergetics Model for the Threespine Stickleback

AbstractThe Threespine Stickleback Gasterosteus aculeatus is widely distributed across northern hemisphere ecosystems, has ecological influence as an abundant planktivore, and is commonly used as a model organism, but the species lacks a comprehensive model to describe bioenergetic performance in response to varying environmental or ecological conditions. This study parameterized a bioenergetics model for the Threespine Stickleback using laboratory measurements to determine mass‐ and temperature‐dependent functions for maximum consumption and routine respiration costs. Maximum consumption experiments were conducted across a range of temperatures from 7.5°C to 23.0°C and a range of fish weights from 0.5 to 4.5 g. Respiration experiments were conducted across a range of temperatures from 8°C to 28°C. Model sensitivity was consistent with other comparable models in that the mass‐dependent parameters for maximum consumption were the most sensitive. Growth estimates based on the Threespine Stickleback bioenergetics model suggested that 22°C is the optimal temperature for growth when food is not limiting. The bioenergetics model performed well when used to predict independent, paired measures of consumption and growth observed from a separate wild population of Threespine Sticklebacks. Predicted values for consumption and growth (expressed as percent body weight per day) only deviated from observed values by 2.0%. Our model should provide insight into the physiological performance of this species across a range of environmental conditions and be useful for quantifying the trophic impact of this species in food webs containing other ecologically or economically important species.

The Effect of Salinity on Egg Development and Viability of Schistocephalus solidus (Cestoda: Diphyllobothriidea).

Schistocephalus solidus plerocercoids commonly infect three-spined stickleback Gasterosteus aculeatus populations in brackish and freshwaters, but infections are typically absent from marine populations. Here we provide an experimental test of the salinity tolerance of S. solidus eggs, to determine the role of salinity in limiting the distribution of infection in coastal zones. We find that S. solidus eggs, derived from the in vitro culture of 3 different plerocercoids, developed normally in salinities of up to 12.5‰, but above this egg viability dropped rapidly, and no egg hatching was observed at salinities above 20‰. Our results are consistent with the distribution of infections in natural stickleback populations and add resolution to previous descriptive observations on salinity tolerance in S. solidus. They also demonstrate that S. solidus presents a novel disease challenge to marine populations of three-spined sticklebacks entering brackish and freshwater environments.

Shoal choice and ultraviolet reflections in stickleback populations from different photic habitats

Grouping is a widespread phenomenon in the animal kingdom and the decision to join a group is a function of individual and environmental conditions, meaning that any advantages and disadvantages have to be pondered constantly. Shoaling decisions in fishes are communicated via a variety of factors, such as colour signals, amongst other ultraviolet (UV) signals. The sensitivity for ultraviolet signals is assumed to be costly and a function of the predominant ecological conditions. The island of North Uist, Scotland, comprises bodies of water that possess great variation in their spectral distribution, especially in the UV spectral range. We examined different populations of three-spined stickleback (Gasterosteus aculeatus L.), which is known to use UV for visual tasks, consisting of three populations from tea-stained lakes and four from clear-water lakes, concerning their preferences to join a shoal viewed under UV-present and UV-absent conditions. Nonreproductively active sticklebacks from tea-stained lakes significantly preferred the shoal under UV-absent conditions, whereas sticklebacks from clear-water lakes did not show a significant preference. Reflection measurements showed that the UV chroma (intensity) of sticklebacks from tea-stained lakes was higher than that of sticklebacks from clear-water, most likely contrasting maximally against the UV-poor background or compensating for a stronger attenuation of the signal.

Widespread positive but weak assortative mating by diet within stickleback populations.

Assortative mating – correlation between male and female traits – is common within populations and has the potential to promote genetic diversity and in some cases speciation. Despite its importance, few studies have sought to explain variation in the extent of assortativeness across populations. Here, we measure assortative mating based on an ecologically important trait, diet as inferred from stable isotopes, in 16 unmanipulated lake populations of three-spine stickleback. As predicted, we find a tendency toward positive assortment on the littoral–pelagic axis, although the magnitude is consistently weak. These populations vary relatively little in the strength of assortativeness, and what variation occurs is not explained by hypothesized drivers including habitat cosegregation, the potential for disruptive selection, costs to choosiness, and the strength of the relationship between diet and body size. Our results support recent findings that most assortative mating is positive, while suggesting that new approaches may be required to identify the environmental variables that drive the evolution of nonrandom mating within populations.

Age and growth of marine three-spined stickleback in the White Sea 50 years after a population collapse

In the early 1960s, the population of White Sea marine three-spined stickleback (Gasterosteus aculeatus), a key forage fish, declined drastically, and the species almost completely disappeared from catches. The population started to recover in the late 1990s, and its abundance has increased exponentially since then. Using contemporary and historical data, we contrast the age structure of spawning stock and fish growth before and after the population decline. Most stickleback spawners in 2009–2011 were 2 and 3 years old, with the 3-year-old fish being more abundant. The proportion of 2-year-old fish in recent catches is higher than that 50 years ago, indicating some rejuvenation of the population after the prolonged decline. Moreover, White Sea sticklebacks in the present population grow faster than those in the 1950s. The observed shifts are concurrent with the long-term changes in the temperature regime in the coastal areas of the White Sea, which determine zooplankton abundance and the duration of the feeding season of fish. The variation in life-history traits among both anadromous and marine stickleback populations within a distribution range was examined. The stickleback showed a considerable interpopulation variation in growth, longevity and age/size at maturity, which appeared generally related to thermal conditions at the marine feeding areas.